Drug discovery of antimicrobial photosensitizers using animal models

Current Pharmaceutical Design

Volumn 17, Issue 13, 2011, Pages 1303-1319

  Sharma, Sulbha K ^a   Dai, Tianhong ^a,b   Kharkwal, Gitika B ^a,b   Huang, Ying Ying ^a,b,c   Huang, Liyi ^a,b,c   de Arce, Vida J Bil ^a   Tegos, George P ^a,b,d   Hamblin, Michael R ^a,b,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c GUANGXI MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Antimicrobial photodynamic therapy; Bioluminescence imaging; Cationic tetrapyrroles; Drug discovery; Mouse models of localized infections; Phenothiazinium dyes; Reactive oxygen species

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; 3,13 BIS [(2 (TRIMETHYLAMMONIO) ETHYLAMINO) CARBONYL] 8,8,18,18 TETRAMETHYLBACTERIOCHLORIN DIIODIDE; 3,13 BIS [3 (BIS (3 TRIMETHYLAMMONIO) PROPYL) AMINOCARBONYL] 8,8,18,18 TETRAMETHYLBACTERIOCHLORIN TETRAIODIDE; 3,13 BIS [3 (BIS (3 TRIMETHYLAMMONIO) PROPYLMETHYLAMMONIO) PROPYLCARBOXAMIDO] 8,8,18,18 TETRAMETHYLBACTERIOCHLORIN HEXAIODIDE; 5 PHENYL 10,15,20 TRIS(N METHYL 4 PYRIDYL) PORPHYRIN CHLORIDE; ANTIINFECTIVE AGENT; BACTERIOCHLORIN; BIS CATIONIC FULLERENE; DIMETHYLMETHYLENE BLUE; FULLERENE DERIVATIVE; HEXAKIS CATIONIC FULLERENE; HYPERICIN; LIPOSOME; METHYLENE BLUE; NANOPARTICLE; NEW METHYLENE BLUE; OCTAKIS CATIONIC GALLIUM 3; PHENOTHIAZINE DERIVATIVE; PHOTOSENSITIZING AGENT; PHTHALOCYANINE DERIVATIVE; PORPHYRIN; RLP 068; TETRA (4N METHYLPYRIDYL) PORPHINE TETRAIODIDE; TETRA (4N,N,N TRIMETHYL ANILINIUM) PORPHINE TETRAIODIDE; TETRAKIS CATIONIC PHTHALOCYANINE; TOLONIUM CHLORIDE; TRIS CATIONIC PORPHYCENE; TRIS METHYL PYRROLIDINIUM FULLERENE; UNCLASSIFIED DRUG; UNINDEXED DRUG; ZINC PYRIDINIUM PHTHALOCYANINE;

BACTERIAL CELL; BIOLUMINESCENCE; BURN INFECTION; CANDIDIASIS; CONJUGATION; DRUG DELIVERY SYSTEM; DRUG STRUCTURE; DRUG SYNTHESIS; EXPERIMENTAL ANIMAL; GRAM NEGATIVE INFECTION; GRAM POSITIVE INFECTION; HUMAN; INFECTION; METHEMOGLOBINEMIA; NEOPLASM; NONHUMAN; PHOTOBIOLOGY; PHOTODYNAMIC THERAPY; POLYMERIZATION; PRIORITY JOURNAL; REVIEW; SKIN ABRASION; SOFT TISSUE INFECTION; WOUND INFECTION;

EID: 79958092702     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161211795703735     Document Type: Review

References (93)

1. Levy JG, Obochi M. New applications in photodynamic therapy. Introduction. Photochem Photobiol 1996; 64: 737-9.
2. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q. Photodynamic therapy. J Natl Cancer Inst 1998; 90: 889-905.
3. Ochsner M. Photophysical and photobiological processes in the photodynamic therapy of tumours. J Photochem Photobiol B 1997; 39: 1-18.
4. Raab O. Über die Wirkung fluoresceinder Stoffe and Infusorien. Zeit für Biol. 1900; 39: 524-546.
5. Wainwright W. Photoantimicrobials-a PACT against resistance and infection. Drug Future 2004; 29: 85-93.
6. Gleckman RABorrego F. Adverse reactions to antibiotics. Clues for recognizing, understanding, and avoiding them. Postgrad Med 1997; 101: 97-8, 101-4, 107-8.
7. Smith TL, Pearson ML, Wilcox KR, Cruz C, Lancaster MV, Robinson-Dunn B, Tenover FC, Zervos MJ, Band JD, White E, Jarvis WR. Emergence of vancomycin resistance in Staphylococcus aureus. Glycopeptide-Intermediate Staphylococcus aureus Working Group. N Engl J Med 1999; 340: 493-501.
8. Minnock A, Vernon DI, Schofield J, Griffiths J, Parish JH, Brown ST. Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-negative and gram-positive bacteria. J Photochem Photobiol B 1996; 32: 159-64.
9. Merchat M, Bertolini G, Giacomini P, Villanueva A, Jori G. Mesosubstituted cationic porphyrins as efficient photosensitizers of gram-positive and gram-negative bacteria. J Photochem Photobiol B 1996; 32: 153-7.
10. Wilson M, Burns T, Pratten J, Pearson GJ. Bacteria in supragingival plaque samples can be killed by low-power laser light in the presence of a photosensitizer. J Appl Bacteriol 1995; 78: 569-74.
11. Malik Z, Hanania J, Nitzan Y. Bactericidal effects of photoactivated porphyrins--an alternative approach to antimicrobial drugs. J Photochem Photobiol B 1990; 5: 281-93.
12. Malik Z, Ladan H, Nitzan Y. Photodynamic inactivation of Gramnegative bacteria: problems and possible solutions. J Photochem Photobiol B 1992; 14: 262-6.
13. Wainwright M. Photoinactivation of viruses. Photochem Photobiol Sci 2004; 3: 406-11.
14. Fuchs BB, Tegos GP, Hamblin MR, Mylonakis E. Susceptibility of Cryptococcus neoformans to photodynamic inactivation is associated with cell wall integrity. Antimicrob Agents Chemother 2007; 51: 2929-36.
15. Bliss JM, Bigelow CE, Foster TH, Haidaris CG. Susceptibility of Candida species to photodynamic effects of photofrin. Antimicrob Agents Chemother 2004; 48: 2000-6.
16. Gonzales FP, da Silva SH, Roberts DW, Braga GU. Photodynamic inactivation of conidia of the fungi Metarhizium anisopliae and Aspergillus nidulans with methylene blue and toluidine blue. Photochem Photobiol 2010; 86: 653-61.
17. Kassab K, Dei D, Roncucci G, Jori G, Coppellotti O. Phthalocyanine-photosensitized inactivation of a pathogenic protozoan, Acanthamoeba palestinensis. Photochem Photobiol Sci 2003; 2: 668-72.
18. Gottlieb P, Shen LG, Chimezie E, Bahng S, Kenney ME, Horowitz B, Ben-Hur E. Inactivation of Trypanosoma cruzi trypomastigote forms in blood components by photodynamic treatment with phthalocyanines. Photochem Photobiol 1995; 62: 869-74.
19. Akilov OE, Kosaka S, O'Riordan K, Song X, Sherwood M, Flotte TJ, Foley JW, Hasan T. The role of photosensitizer molecular charge and structure on the efficacy of photodynamic therapy against Leishmania parasites. Chem Biol 2006; 13: 839-47.
20. Phoenix DA, Sayed Z, Hussain S, Harris F, Wainwright M. The phototoxicity of phenothiazinium derivatives against Escherichia coli and Staphylococcus aureus. FEMS Immunol Med Microbiol 2003; 39: 17-22.
21. Wainwright M, Phoenix DA, Marland J, Wareing DR, Bolton FJ. A study of photobactericidal activity in the phenothiazinium series. FEMS Immunol Med Microbiol 1997; 19: 75-80.
22. Wainwright MCrossley KB. Methylene Blue--a therapeutic dye for all seasons? J Chemother 2002; 14: 431-43.
23. Wainwright M. 'Safe' photoantimicrobials for skin and soft-tissue infections. Int J Antimicrob Agents 2010; 36: 14-8.
24. Ragas X, Dai T, Tegos GP, Agut M, Nonell S, Hamblin MR. Photodynamic inactivation of Acinetobacter baumannii using phenothiazinium dyes: in vitro and in vivo studies. Lasers Surg Med 2010; 42: 384-90.
25. O'Neill J, Wilson M, Wainwright M. Comparative antistreptococcal activity of photobactericidal agents. J Chemother 2003; 15: 329-34.
26. Wainwright M, Phoenix DA, Rice L, Burrow SM, Waring J. Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation. J Photochem Photobiol B 1997; 40: 233-9.
27. Tegos GPHamblin MR. Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps. Antimicrob Agents Chemother 2006; 50: 196-203.
28. Tegos GP, Masago K, Aziz F, Higginbotham A, Stermitz FR, Hamblin MR. Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation. Antimicrob Agents Chemother 2008; 52: 3202-9.
29. Foley JW, Song X, Demidova TN, Jalil F, Hamblin MR. Synthesis and properties of benzo[a]phenoxazinium chalcogen analogues as novel broad-spectrum antimicrobial photosensitizers. J Med Chem 2006; 49: 5291-9.
30. Smijs TG, Pavel S, Talebi M, Bouwstra JA. Preclinical studies with 5,10,15-Tris(4-methylpyridinium)-20-phenyl-[21H,23H]-porphine trichloride for the photodynamic treatment of superficial mycoses caused by Trichophyton rubrum. Photochem Photobiol 2009; 85: 733-9.
31. Lambrechts SA, Aalders MC, Van Marle J. Mechanistic study of the photodynamic inactivation of Candida albicans by a cationic porphyrin. Antimicrob Agents Chemother 2005; 49: 2026-34.
32. Lambrechts SA, Aalders MC, Langeveld-Klerks DH, Khayali Y, Lagerberg JW. Effect of monovalent and divalent cations on the photoinactivation of bacteria with meso-substituted cationic porphyrins. Photochem Photobiol 2004; 79: 297-302.
33. Maisch T, Bosl C, Szeimies RM, Lehn N, Abels C. Photodynamic effects of novel XF porphyrin derivatives on prokaryotic and eukaryotic cells. Antimicrob Agents Chemother 2005; 49: 1542-52.
34. Ooi N, Miller K, Randall C, Rhys-Williams W, Love W, Chopra I. XF-70 and XF-73, novel antibacterial agents active against slowgrowing and non-dividing cultures of Staphylococcus aureus including biofilms. J Antimicrob Chemother 2010; 65: 72-8.
35. Ooi N, Miller K, Hobbs J, Rhys-Williams W, Love W, Chopra I. XF-73, a novel antistaphylococcal membrane-active agent with rapid bactericidal activity. J Antimicrob Chemother 2009; 64: 735-40.
36. Banfi S, Caruso E, Buccafurni L, Battini V, Zazzaron S, Barbieri P, Orlandi V. Antibacterial activity of tetraaryl-porphyrin photosensitizers: an in vitro study on Gram negative and Gram positive bacteria. J Photochem Photobiol B 2006; 85: 28-38.
37. Alves E, Costa L, Carvalho CM, Tome JP, Faustino MA, Neves MG, Tome AC, Cavaleiro JA, Cunha A, Almeida A. Charge effect on the photoinactivation of Gram-negative and Gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiol 2009; 9: 70.
38. Carvalho CM, Gomes AT, Fernandes SC, Prata AC, Almeida MA, Cunha MA, Tome JP, Faustino MA, Neves MG, Tome AC, Cavaleiro JA, Lin Z, Rainho JP, Rocha J. Photoinactivation of bacteria in wastewater by porphyrins: bacterial beta-galactosidase activity and leucine-uptake as methods to monitor the process. J Photochem Photobiol B 2007; 88: 112-8.
39. Costa L, Carvalho CM, Faustino MA, Neves MG, Tome JP, Tome AC, Cavaleiro JA, Cunha A, Almeida A. Sewage bacteriophage inactivation by cationic porphyrins: influence of light parameters. Photochem Photobiol Sci 2010; 9: 1126-33.
40. Grinholc M, Kawiak A, Kurlenda J, Graczyk A, Bielawski KP. Photodynamic effect of protoporphyrin diarginate (PPArg2) on methicillin-resistant Staphylococcus aureus and human dermal fibroblasts. Acta Biochim Pol 2008; 55: 85-90.
41. Mantareva V, Kussovski V, Angelov I, Borisova E, Avramov L, Schnurpfeil G, Wohrle D. Photodynamic activity of water-soluble phthalocyanine zinc(II) complexes against pathogenic microorganisms. Bioorg Med Chem 2007; 15: 4829-35.
42. Mantareva V, Kussovski V, Angelov I, Wohrle D, Dimitrov R, Popova E, Dimitrov S. Non-aggregated Ga(iii)-phthalocyanines in the photodynamic inactivation of planktonic and biofilm cultures of pathogenic microorganisms. Photochem Photobiol Sci 2010.
43. Giuliani F, Martinelli M, Cocchi A, Arbia D, Fantetti L, Roncucci G. In vitro resistance selection studies of RLP068/Cl, a new Zn(II) phthalocyanine suitable for antimicrobial photodynamic therapy. Antimicrob Agents Chemother 2010; 54: 637-42.
44. Huang L, Huang YY, Mroz P, Tegos GP, Zhiyentayev T, Sharma SK, Lu Z, Balasubramanian T, Krayer M, Ruzie C, Yang E, Kee HL, Kirmaier C, Diers JR, Bocian DF, Holten D, Lindsey JS, Hamblin MR. Stable synthetic cationic bacteriochlorins as selective antimicrobial photosensitizers. Antimicrob Agents Chemother 2010; 54: 3834-41.
45. Nakamura EIsobe H. Functionalized fullerenes in water. The first 10 years of their chemistry, biology, and nanoscience. Acc Chem Res 2003; 36: 807-15.
46. Tegos GP, Demidova TN, Arcila-Lopez D, Lee H, Wharton T, Gali H, Hamblin MR. Cationic fullerenes are effective and selective antimicrobial photosensitizers. Chem Biol 2005; 12: 1127-35.
47. Huang L, Terakawa M, Zhiyentayev T, Huang YY, Sawayama Y, Jahnke A, Tegos GP, Wharton T, Hamblin MR. Innovative cationic fullerenes as broad-spectrum light-activated antimicrobials. Nanomedicine 2010; 6: 442-52.
48. Spesia MB, Milanesio ME, Durantini EN. Synthesis, properties and photodynamic inactivation of Escherichia coli by novel cationic fullerene C60 derivatives. Eur J Med Chem 2008; 43: 853-61.
49. Stockert JC, Canete M, Juarranz A, Villanueva A, Horobin RW, Borrell JI, Teixido J, Nonell S. Porphycenes: facts and prospects in photodynamic therapy of cancer. Curr Med Chem 2007; 14: 997-1026.
50. Ragas X, Sanchez-Garcia D, Ruiz-Gonzalez R, Dai T, Agut M, Hamblin MR, Nonell S. Cationic Porphycenes as Potential Photosensitizers for Antimicrobial Photodynamic Therapy. J Med Chem 2010.
51. McDonnell SO, Hall MJ, Allen LT, Byrne A, Gallagher WM, O'Shea DF. Supramolecular photonic therapeutic agents. J Am Chem Soc 2005; 127: 16360-1.
52. Frimannsson DO, Grossi M, Murtagh J, Paradisi F, O'Shea DF. Light induced antimicrobial properties of a brominated boron difluoride (BF(2) chelated tetraarylazadipyrromethene photosensitizer. J Med Chem 2010; 53: 7337-43.
53. Hager B, Strauss WS, Falk H. Cationic hypericin derivatives as novel agents with photobactericidal activity: synthesis and photodynamic inactivation of Propionibacterium acnes. Photochem Photobiol 2009; 85: 1201-6.
54. Soukos NS, Hamblin MR, Hasan T. The effect of charge on cellular uptake and phototoxicity of polylysine chlorin(e6) conjugates. Photochem Photobiol 1997; 65: 723-9.
55. Soukos NS, Ximenez-Fyvie LA, Hamblin MR, Socransky SS, Hasan T. Targeted antimicrobial photochemotherapy. Antimicrob Agents Chemother 1998; 42: 2595-601.
56. Hamblin MR, O'Donnell DA, Murthy N, Rajagopalan K, Michaud N, Sherwood ME, Hasan T. Polycationic photosensitizer conjugates: effects of chain length and Gram classification on the photodynamic inactivation of bacteria. J Antimicrob Chemother 2002; 49: 941-951.
57. Tegos GP, Anbe M, Yang C, Demidova TN, Satti M, Mroz P, Janjua S, Gad F, Hamblin MR. Protease-stable polycationic photosensitizer conjugates between polyethyleneimine and chlorin(e6) for broad-spectrum antimicrobial photoinactivation. Antimicrob Agents Chemother 2006; 50: 1402-10.
58. Dai T, Tegos GP, Zhiyentayev T, Mylonakis E, Hamblin MR. Photodynamic therapy for methicillin-resistant Staphylococcus aureus infection in a mouse skin abrasion model. Lasers Surg Med 2010; 42: 38-44.
59. Dai T, Tegos GP, Lu Z, Huang L, Zhiyentayev T, Franklin MJ, Baer DG, Hamblin MR. Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob Agents Chemother 2009; 53: 3929-34.
60. Garcez AS, Nunez SC, Hamblin MR, Ribeiro MS. Antimicrobial effects of photodynamic therapy on patients with necrotic pulps and periapical lesion. J Endod 2008; 34: 138-42.
61. Garcez AS, Ribeiro MS, Tegos GP, Nunez SC, Jorge AO, Hamblin MR. Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection. Lasers Surg Med 2007; 39: 59-66.
62. Demidova TNHamblin MR. Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 2005; 49: 2329-35.
63. Gad F, Zahra T, Hasan T, Hamblin MR. Effects of growth phase and extracellular slime on photodynamic inactivation of grampositive pathogenic bacteria. Antimicrob Agents Chemother 2004; 48: 2173-8.
64. Gad F, Zahra T, Francis KP, Hasan T, Hamblin MR. Targeted photodynamic therapy of established soft-tissue infections in mice. Photochem Photobiol Sci 2004; 3: 451-8.
65. Hamblin MR, Zahra T, Contag CH, McManus AT, Hasan T. Optical monitoring and treatment of potentially lethal wound infections in vivo. J Infect Dis 2003; 187: 1717-25.
66. Hamblin MR, O'Donnell DA, Murthy N, Contag CH, Hasan T. Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem Photobiol 2002; 75: 51-7.
67. Polo L, Segalla A, Bertoloni G, Jori G, Schaffner K, Reddi E. Polylysine-porphycene conjugates as efficient photosensitizers for the inactivation of microbial pathogens. J Photochem Photobiol B 2000; 59: 152-8.
68. Lauro FM, Pretto P, Covolo L, Jori G, Bertoloni G. Photoinactivation of bacterial strains involved in periodontal diseases sensitized by porphycene-polylysine conjugates. Photochem Photobiol Sci 2002; 1: 468-70.
69. Rovaldi CR, Pievsky A, Sole NA, Friden PM, Rothstein DM, Spacciapoli P. Photoactive porphyrin derivative with broadspectrum activity against oral pathogens In vitro. Antimicrob Agents Chemother 2000; 44: 3364-7.
70. Bombelli C, Bordi F, Ferro S, Giansanti L, Jori G, Mancini G, Mazzuca C, Monti D, Ricchelli F, Sennato S, Venanzi M. New cationic liposomes as vehicles of m-tetrahydroxyphenylchlorin in photodynamic therapy of infectious diseases. Mol Pharm 2008; 5: 672-9.
71. Ferro S, Ricchelli F, Mancini G, Tognon G, Jori G. Inactivation of methicillin-resistant Staphylococcus aureus (MRSA) by liposomedelivered photosensitising agents. J Photochem Photobiol B 2006; 83: 98-104.
72. Schwiertz J, Wiehe A, Grafe S, Gitter B, Epple M. Calcium phosphate nanoparticles as efficient carriers for photodynamic therapy against cells and bacteria. Biomaterials 2009; 30: 3324-31.
73. Ferro S, Jori G, Sortino S, Stancanelli R, Nikolov P, Tognon G, Ricchelli F, Mazzaglia A. Inclusion of 5-[4-(1-dodecanoylpyridinium)]-10,15,20-triphenylporphine in supramolecular aggregates of cationic amphiphilic cyclodextrins: physicochemical characterization of the complexes and strengthening of the antimicrobial photosensitizing activity. Biomacromolecules 2009; 10: 2592-600.
74. Ferro S, Ricchelli F, Monti D, Mancini G, Jori G. Efficient photoinactivation of methicillin-resistant Staphylococcus aureus by a novel porphyrin incorporated into a poly-cationic liposome. Int J Biochem Cell Biol 2007; 39: 1026-34.
75. Lu XM, Fischman AJ, Stevens E, Lee TT, Strong L, Tompkins RG, Yarmush ML. Sn-chlorin e6 antibacterial immunoconjugates. An in vitro and in vivo analysis. J Immunol Methods 1992; 156: 85-99.
76. Friedberg JS, Tompkins RG, Rakestraw SL, Warren SW, Fischman AJ, Yarmush ML. Antibody-targeted photolysis. Bacteriocidal effects of Sn (IV) chlorin e6-dextran-monoclonal antibody conjugates. Ann N Y Acad Sci 1991; 618: 383-93.
77. Berthiaume F, Reiken SR, Toner M, Tompkins RG, Yarmush ML. Antibody-targeted photolysis of bacteria in vivo. Biotechnology (N Y) 1994; 12: 703-6.
78. Demidova TN, Gad F, Zahra T, Francis KP, Hamblin MR. Monitoring photodynamic therapy of localized infections by bioluminescence imaging of genetically engineered bacteria. J Photochem Photobiol B 2005; 81: 15-25.
79. Rocchetta HL, Boylan CJ, Foley JW, Iversen PW, LeTourneau DL, McMillian CL, Contag PR, Jenkins DE, Parr TR, Jr. Validation of a noninvasive, real-time imaging technology using bioluminescent Escherichia coli in the neutropenic mouse thigh model of infection. Antimicrob Agents Chemother 2001; 45: 129-37.
80. Francis KP, Joh D, Bellinger-Kawahara C, Hawkinson MJ, Purchio TF, Contag PR. Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect Immun 2000; 68: 3594-600.
81. Francis KP, Yu J, Bellinger-Kawahara C, Joh D, Hawkinson MJ, Xiao G, Purchio TF, Caparon MG, Lipsitch M, Contag PR. Visualizing pneumococcal infections in the lungs of live mice using bioluminescent Streptococcus pneumoniae transformed with a novel gram-positive lux transposon. Infect Immun 2001; 69: 3350-8.
82. Latorre-Esteves E, Akilov OE, Rai P, Beverley SM, Hasan T. Monitoring the efficacy of antimicrobial photodynamic therapy in a murine model of cutaneous leishmaniasis using L. major expressing GFP. J Biophotonics 2010; 3: 328-35.
83. Hamblin MRDai T. Can surgical site infections be treated by photodynamic therapy? Photodiagnosis Photodyn Ther 2010; 7: 134-6.
84. Lu Z, Dai T, Huang L, Kurup DB, Tegos GP, Jahnke A, Wharton T, Hamblin MR. Photodynamic therapy with a cationic functionalized fullerene rescues mice from fatal wound infections. Nanomedicine (UK) 2010; 5: in press.
85. Lambrechts SA, Demidova TN, Aalders MC, Hasan T, Hamblin MR. Photodynamic therapy for Staphylococcus aureus infected burn wounds in mice. Photochem Photobiol Sci 2005; 4: 503-9.
86. Ragas X, Dai T, Tegos GP, Agut M, Nonell S, Hamblin MR. Photodynamic inactivation of Acinetobacter baumannii using phenothiazinium dyes: in-vitro and in-vivo studies. Lasers Surg Med 2010; in press.
87. Bowers AL, Huffman GR, Sennett BJ. Methicillin-resistant Staphylococcus aureus infections in collegiate football players. Med Sci Sports Exerc 2008; 40: 1362-7.
88. Turbeville SD, Cowan LD, Greenfield RA. Infectious disease outbreaks in competitive sports: a review of the literature. Am J Sports Med 2006; 34: 1860-5.
89. Kirkland EB Adams BB. Methicillin-resistant Staphylococcus aureus and athletes. J Am Acad Dermatol 2008; 59: 494-502.
90. Doyle TC, Nawotka KA, Purchio AF, Akin AR, Francis KP, Contag PR. Expression of firefly luciferase in Candida albicans and its use in the selection of stable transformants. Microb Pathog 2006; 40: 69-81.
91. Doyle TC, Nawotka KA, Kawahara CB, Francis KP, Contag PR. Visualizing fungal infections in living mice using bioluminescent pathogenic Candida albicans strains transformed with the firefly luciferase gene. Microb Pathog 2006; 40: 82-90.
92. Saville SP, Lazzell AL, Chaturvedi AK, Monteagudo C, Lopez-Ribot JL. Use of a genetically engineered strain to evaluate the pathogenic potential of yeast cell and filamentous forms during Candida albicans systemic infection in immunodeficient mice. Infect Immun 2008; 76: 97-102.
93. Robert VA, Casadevall A. Vertebrate endothermy restricts most fungi as potential pathogens. J Infect Dis 2009; 200: 1623-6.